accreta placentation: a systematic review of prenatal ......key words: placenta, accreta, increta,...
TRANSCRIPT
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Accreta Placentation: A systematic review of Prenatal Ultrasound Imaging and Grading of Villous Invasiveness Eric JAUNIAUX1,MD,PhD Sally L COLLINS2,MBBS,PhD Davor JURKOVIC1,MD Graham J BURTON3,MD
1. Department of Obstetrics and Gynaecology, University College London Hospitals and UCL Institute for Women’s Health, University College London (UCL), London, UK.
2. Nuffield Department of Obstetrics & Gynaecology, University of Oxford, and the Fetal Medicine Unit, John Radcliffe Hospital, Oxford, UK
3. The Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.
The authors report no conflict of interest No funding was obtained for this study. Corresponding author: Professor Eric Jauniaux, Academic Department of Obstetrics and Gynaecology, Institute for Women’s Health, University College London, 86-96 Chenies Mews, London WC1E 6HX, UK. Telephone numbers: +44/207/3908113 Fax: +44/207/3908115 E-mail: [email protected] Word count: 4250 Condensation: Heterogeneity in terminology and study designs on ultrasound diagnosis of placenta accreta limit the evaluation of the depth of myometrial villous invasion and management strategies Short title: Grading of accreta placenta on ultrasound imaging
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Abstract Objective: Determining the depth of villous invasiveness before delivery is pivotal in
planning individual management of placenta accreta (PA). We have evaluate the value
of the various ultrasound signs described in the literature for the diagnosis of PA and in
the assessment of the depth of villous invasiveness.
Data sources: We undertook a PubMed and MEDLINE search of the relevant studies
published between the first prenatal ultrasound description of PA in 1982 and 30 March
2016 using key words “placenta accreta”, “placenta increta”, “placenta percreta”,
“abnormally invasive placenta”, “morbidly adherent placenta” and “placenta adhesive
disorder” as related to “sonography”, “ultrasound diagnosis”, “prenatal diagnosis”, “grey-
scale imaging”, three-dimensional (3D) ultrasound and “colour Doppler imaging”.
Study eligibility criteria: All articles which correlated prenatal ultrasound imaging with
pregnancy outcome.
Study appraisal and synthesis methods: Eighty-three studies, including 30 cases
reports describing 38 cases of PA and 53 series describing 1078 cases were analysed.
PA was subdivided in placenta creta (PC) to describe superficially adherent placentation
and placenta increta (PI) and percreta (PP) to describe invasive placentation.
Results: Out of 53 study series, 23 did not provide data on the depth of villous
myometrial invasion on ultrasound imaging or at delivery. Detailed correlations between
ultrasound findings and PA grading were found in 72 cases. A loss of clear zone
(62.1%) and the presence of bridging vessels (71.4%) were the most common
ultrasound signs found in cases of PC. In PI, a loss of clear zone (84.6%) and
subplacental hypervascularity (60%) were the most common ultrasound signs whereas,
placental lacunae (82.4%) and subplacental hypervascularity (54.5%) were the most
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common ultrasound signs in PP. No ultrasound sign or a combination of ultrasound
signs were specific of the depth of accreta placentation.
Conclusions: The wide heterogeneity in terminology used to describe the grades of
accreta placentation and differences in study design limits the evaluation of the
accuracy of ultrasound imaging in the screening and diagnosis of PA. This review
emphasizes the need for further prospective studies using a standardised evidence-
based approach including a systematic correlation between ultrasound signs of PA and
detailed clinical and pathologic examinations at delivery.
Key words: Placenta, accreta, increta, percreta, ultrasound imaging, villous myometrial invasion, accreta placentation.
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Introduction
Placenta accreta (PA) is an iatrogenic 20th century disorder of human placentation,
which is characterized by the abnormal attachment or invasion of placental tissue to the
underlying uterine musculature.1 PA may have been observed before the 20th century6
but all epidemiologic studies have shown a direct association between the increase in
caesarean delivery (CD) and the increased incidence of PA in subsequent pregnancies.
1,3-7 PA is not exclusively a consequence of CD and much smaller surgical damage to
the integrity of the uterine lining, such as following uterine curettage, manual delivery of
the placenta, post-partum endometritis and previous hysteroscopic surgery, endometrial
resection and uterine artery embolization, has been associated with PA in subsequent
pregnancies. 1,3-8 The development of PA has also been reported in women with no
surgical history but presenting with uterine pathology such as bicornuate uterus,
adenomyosis, submucous fibroids and myotonic dystrophy.1,3,4 These individual case
reports, suggest that intra-myometrial implantation of villous tissue is not always
secondary to uterine surgery and may explain the few cases rare cases of PA observed
before the 20th century.
PA was first defined in 1937 by Irving and Hertig, as the “abnormal adherence of
the afterbirth in whole or in parts to the underlying uterine wall”.2 The failure of the
placenta to separate normally from the uterus after delivery is typically accompanied by
severe postpartum haemorrhage (PPH), and attempts to remove a PA typically
provokes further major haemorrhage which is associated with increased maternal
morbidity and mortality. Modern pathologists have graded PA into placenta creta (PC)
or vera, placenta increta (PI) and placenta percreta (PP) according to the depth of
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villous invasiveness.3,4 In PC, the villi adhere to the myometrium with no intermediate
decidual layers between the tip of the anchoring villi and the muscular cells but do not
invade the myometrium. In PI, the villi penetrate deeply into the myometrium up to the
external layer whereas in PP, the invasive villous tissue reaches and/or penetrates
through the uterine serosa. The PA spectrum can therefore be subdivided into PC for
abnormally adherent placentation and PI and PP for abnormally invasive placentation.
Cases of PA are also often subdivided into total, partial or focal according the amount of
placental issue involved. More recently, it has been suggested that cesarean scar
pregnancy CSP represents a precursor of one of the different grades of PA10-12
Several concepts have been proposed to explain the pathophysiology of PA. The
oldest is based on a theoretical primary defect of the biological functions of the
trophoblast, leading to excessive adherence or invasion of the myometrium. The other
prevailing hypothesis is that of a secondary defect of the endometrium-myometrial
interface leading to a failure of normal decidualization in the area of the uterine scar
allowing trophoblastic infiltration beyond the superficial myometrium and villous
development inside the myometrium.1,3,4 Although, the pathogenic mechanisms of the
different types of accreta placentation, including scar pregnancies, are similar, the
anatomical and clinical consequences vary widely. In placenta vera, the villi simply
adhere to the superficial layer of the myometrium whereas in placenta increta and
percreta the villous tissue invades into and may penetrate through the entire uterine wall
thickness and reach the surrounding pelvic tissues and organs.
The worst clinical outcome arises when PA and in particular, when PI or PP is
unsuspected at the time of delivery and the surgeon attempts to remove the invasive
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part of the placenta leading immediately to major haemorrhage and an increasing need
for emergency hysterectomy.13-15 Prenatal diagnosis of PA has therefore become
essential for the safe management of this increasingly common obstetric
complication.16-18 However, recent studies from UK and USA show that PA was
undiagnosed before delivery in between half19 and a third20 of the cases. Determining
the depth of placental invasion is essential for planning of individual management of
women diagnosed with PA.
The objective of this review is to evaluate the value of the various ultrasound
signs described in the international literature for the diagnosis of PA in general and for
the assessment of the depth of villous invasiveness in the uterine wall in particular.
Methods
Information sources and search strategy
We conducted a systematic review of the literature and selected relevant studies that
have been published between the first prenatal ultrasound description of PA by Tabsh
et al22 in 1982 and 30 March 2016. We undertook a PubMed and MEDLINE search
using combinations of key words of “placenta accreta”, “placenta creta”, “placenta
increta”, placenta percreta”, “abnormally invasive placenta”, “morbidly adherent
placenta” and “placenta adhesive disorder” as related to “sonography”, “ultrasound
diagnosis”, “prenatal diagnosis”, “grey-scale imaging”, three-dimensional (3D)
ultrasound and “colour Doppler imaging.” We limited the search to studies published in
English.
Eligibility creteria
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The primary eligibility criteria were articles which correlated prenatal ultrasound imaging
with pregnancy outcome. We used ultrasound signs from the standardized descriptions
proposed recently by the European Working Group on Abnormally Invasive Placenta
(EW-AIP) and the AIP international expert group.23,24 On gray-scale imaging the signs of
PA are: loss of the clear zone in the myometrium under the placental bed (“clear zone”);
myometrial thinning to
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describe superficially adherent placentation and placenta increta (PI) and percreta (PP)
to describe invasive placentation.
Synthesis of results
Data containing study setting, study type, characteristics of study population, definition
of PA, terminology, grading, ultrasound description of placental structure were obtained
for each 83 studies selected. To evaluate the relationships between the depth of villous
invasiveness, ultrasound signs and clinical findings management procedures including
caesarean section hysterectomy (CSHT), focal myometrial resection (FMR), uterine
artery embolization (UAE), uterine artery balloon occlusion (UABO), uterine artery
ligation (UAL) intrauterine balloon tamponade, methotrexate (MTX), B-Lynch suture and
lesions described during pathological examination were also extracted.
The case reports data were analysed using the StatGraphic data analysis and
statistical software package (Manugistics, Rockville, MD).
Results
Case reports characteristics
The case reports included 38 individual cases with prenatal ultrasound findings. There
were four case reports presenting findings on 2 individual cases25,34,36,45 and one
including 3 individual cases.46 The PA grading was confirmed clinically or
histopathologically as PC in 13 cases, PI in 16 cases and PP in 9 cases.
A planned CD hysterectomy with or without UAE or UAL was performed in two
PC, nine PI and seven PP.20,22,32,35-39,41,46,48,52,53 In the other 20 cases a conservative
management was attempted including FMR with or without suture or MTX29,31,34,43,46,50
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uterine curettage55 and the placental left in situ with MTX or UAE.25,27,28,30,41,42,45-47,49,51
The conservative management was unsuccessful in 12 cases, including five PC, 6 PI
and one PP, and required a secondary hysterectomy.25,27,28,30,34,41,42,44,45,49,55 A
dissection or partial resection of the bladder was required in four cases of PP.33,35,42,54
The mean gestational age at delivery was 30.6 weeks (SD: 7.5; range 15-39 weeks). A
detailed description of the pathologic findings was available in 28 cases. In the
remaining 10 cases it was not available following successful conservative management
but the PA grading was described at delivery.
Case reports synthesis of results
The terminology “placenta accreta” was used by 27 authors of case reports 25-44,46-48,50-
52,54,55, “morbidly adherent placenta” by two45,49 and “abnormal placentation” in one
report.53 Two authors reporting on three cases did not describe the past surgical
history.25,40 In five (14.3%) cases there was a previous history of uterine curettage
only28,30,31,50,51 and in seven (20.0%) the women presented with a combined history of
CD, myomectomy and/or curettage.30,32,36,39,45,46,55 A past obstetric history of CD was
reported in 23 out of 35 remaining cases (65.7%).
Gray-scale imaging was used by all authors. In eight cases, including two PC,
five PI and one PP only gray-scale imaging signs were described25,27,33,47,48,52,55
whereas in the remaining 30 cases, including 11 PC, 11 PI and eight PP, both gray-
scale and color Doppler imaging were reported. Table 1 displays the ultrasound signs
identified in the diagnosis of the 38 cases reports included in the review according to the
depth of villous myometrial invasion. The mean gestational age at diagnosis was 24.3
weeks (SD: 6.8; range 13-36 weeks). A loss of clear zone (92.3%) and bridging vessels
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(90.9%) were the most common ultrasound signs for PC. In cases of PI, the loss of
clear zone (87.5%) and subplacental hypervascularity (81.8%) were the most common
signs whereas for PP, placental lacunae were found in all cases (100%) and
subplacental hypervascularity was found in six cases (75%).
Series characteristics
The 53 series included 24 prospective58-62,65,66,70-72,76,80,83,85,89-91,93,98,101,102,105-107 and 29
retrospective studies with a total of 1078 cases of PA. All series except eight, which did
not report data on previous surgical history63,66,72,81,97,98,101,106, included women
presenting with placenta praevia and a history of CD and/or other uterine surgeries. In
21 series, including 568 cases of PA, the depth of villous invasiveness was not
described.20,59,66-69,71,72,75,76,78,81,82,85,90,91,94,96,100,104,106. In the other 32 series, the
distribution of the different categories of PA were reported, including 240 PC, 112 PI
and 158 PP.
A planned CD hysterectomy, with or without UAE or UAL, was the primary
management option in 44 series. In 13 series, conservative management was
attempted depending on the degree of myometrial invasion with secondary
hysterectomy in cases of failure20,56,62,63,71,73,75,80,84,87,92,95,97 and in one series
conservative management was successful in all cases.99 In seven series, no information
was available on the outcome and management.20,65,85,91,98,100,107 Overall, a CD
hysterectomy was performed in 597 out of 806 (74.1%) for which the data were
available. The mean gestational age range at delivery was 34-37 weeks. A detailed
description of the pathologic findings was available in 29 series. In 11 series, the
pathologic examination was reported as performed but no data were
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provided58,59,65,67,69,81,82,87,100,104,106 and in 12 series there was no histopathologic
information.20,56,68,75,85,90,91,95,96,98,99,103
Series synthesis of results
The terminology used to describe PA was diverse. Seven studies used the term
“morbidly adherent placenta”66,86,89,97,100,103,106, two used “placental adhesive
disorders”70,101, two used “abnormally invasive placentation” 92,104, two used “abnormally
adherent placenta” or “abnormal placental adherence”79,83, one use “advanced invasive
placentation”96 and one used the term “abnormal myometrial invasion”.61
Gray-scale ultrasound was used, and the corresponding data presented by all
authors except one.104 In ten series, gray-scale imaging only was used56-
58,64,65,75,84,89,90,103, in one series sequential two- dimensional (2D) and three-dimensional
(3D) ultrasound were used.77 In the remaining 41 series, data from both 2D grey-scale
ultrasound and CDI were available. The gestational mean range at diagnosis in 31
series for which the information was available was 20-34 weeks. Table 2 displays the
ultrasound signs used by authors to diagnosed PA in the 53 series. The most commonly
used signs were loss of clear zone (98%) and placental lacunae (96.1) for grey-scale
imaging and subplacental hypervascularity (85.7%) and bridging vessels (61.9%) for
CDI. The authors of eight series provided detailed data on 2D ultrasound examination
and placental grading.65,79,84,89,95,98,102,107 The corresponding data are presented in Table
3. The presence of placental lacunae (78.9%) and subplacental hypervascularity
(36.7%) were the most common ultrasound signs found. In three of these series65,84,102
the authors provided details of the placental grading for each individual standard
ultrasound sign. These data were combined with those from the cases reports (Table 4)
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raising the number of cases available for analysis to 72. This analysis confirmed that a
loss of clear zone (62.1%) and the presence of bridging vessels (71.4%) were the most
common ultrasound signs found in cases of PC, that a loss of clear zone (84.6%) and
subplacental hypervascularity (60%) were the most common sings in PI whereas
placental lacunae (82.4%) and subplacental hypervascularity (54.5%) were the most
common signs for PP. There were no ultrasound sign or combination of ultrasound
signs were specific of the depth of accreta placentation. No series reported on the
lateral extension of the accreta placentation and in particular on the involvement of the
cervix.
Comments
Main findings
Although some ultrasound signs are more often associated with PA, no ultrasound sign
or combination of ultrasound signs are specific of the depth of accreta placentation. The
wide heterogeneity in terminology and study designs in the published reports on the
prenatal ultrasound diagnosis of PA could explain the low detection rate during routine
ultrasound examination.
Comparison with existing literature
The origin and first use of the terminology “placenta accreta” is unknown. Langhans108
and Hart 109, who first described the histology of PA, also used the term “adherent
placenta”. On the basis that the depth of the villous penetration of the myometrium is
rarely uniform, Luke et al, suggested the name “adherent or invasive placenta” instead
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of PA21 and the first author to use to term “placenta accreta” was Baisch in 1907.110 Up
to the 1920s, most authors used the term “adherent placenta”, whereas after that and
until the present review most authors used placenta “accreta” or “increta” whereas the
term “percreta” was only used regularly to describe case reports from the 1950s
onwards.111 By contrast, the term “morbidly adherent placenta” dates back to the 19th
century to describe placental retention112, and has been very rarely used to describe PA
until recently. Our review finds that this terminology has been increasingly used over the
last decade, by authors of case reports and series of prenatal ultrasound diagnosis of
PA to describe both abnormally adherent and invasive placentas.45,49,66,86,89,97,100,103,106
This terminology is inaccurate and misleading and for our analysis of the literature we
have used the standard anatomical definition i.e. creta, increta & percreta which
describes accurately the depth spectrum of villous myometrial invasion.
Only one of the 20 cases personally treated by Irving and Hertig occurred after a
previous CD.9 Similarly, in their review of 86 cases reports up to 1935, only one was
found after a CD. Predisposing factors at the time were a previous manual delivery
and/or “vigorous” uterine curettage. Three decades later, CD was found in the history of
around half of the women presenting with PC or PI in subsequent pregnancy.21 In the
present review and in population studies, a history of one or more CD is reported as the
main predisposing factor in more than 90% of the cases of PA.5-7,13,14 The risks of both
placenta praevia and PA in subsequent pregnancies increase with the number of
previous CD7,13,114 and is higher in women with a previous classical CD.115 Among
women with placenta praevia, 40% of those with two previous CD and 61% of those
with three previous CD develop a PA.7 This risk is independent of other maternal
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characteristics, such as parity, body mass index, tobacco use, and coexisting
hypertension or diabetes. Although PA only complicates about 5% of pregnancies with
placenta praevia13, and around 0.5% of women undergoing their second or third CD114,
the identification during the second trimester of a placenta praevia on ultrasound
examination in a woman with a history of CD should prompt a more detailed search for
signs of PA and evaluation of the depth of villous myometrial invasion.
The first antenatal grey-scale imaging descriptions of PA were reported 25 years
ago by Tabsh et al22 and ultrasonography is now the most commonly used modality for
diagnosing PA. The first ultrasound sign described was the “loss of the hypoechoic
retroplacental (clear) zone” found to represent an abnormal extension of the placental
villi through the decidua basalis into the myometrium.25,56 This probably corresponds the
placental basal plate or utero-placental plate described by placental anatomists.3,4 In
1992, Finberg and Williams58 using higher resolution grey-scale imaging identified
further signs including marked thinning or absence of the myometrial zone; thinning,
irregularity, or focal disruption of the utero-placental bladder zone; intraplacental
vascular lacunae and presence of focal mass-like elevations or extension of placental
echogenicity (exophytic) beyond the uterine serosa. The advent of CDI enabled access
to visualization of the utero-placental circulation, and indicated that most cases of PA
are associated with hypervascularisation patterns within the placenta and below the
placental bed or subplacental zone.25 Our review indicates that these signs have been
commonly used since their first description and that the loss of clear zone, the presence
of placental lacunae and hypervascularity of the subplacental zone were the most
frequently found ultrasound signs in PA (Table 3). When analyzed for the depth of
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villous myometrial invasion, a loss of clear zone was the most common grey-scale
imaging sign found for PC and PI and the presence of placental lacunae for PP. On
CDI, bridging vessels are more commonly reported in PC, whereas subplacental
hypervascularity was the most common sign found in PI and PP (Table 4). Although
placental lacunae were reported in all case reports of PP (Table 1), we found that no
ultrasound sign or combination of ultrasound signs were specific of the depth of accreta
placentation. This can be explained by the absence of standardised description of
ultrasound signs in previous studies, the high proportion of retrospective studies and the
lack of PA grading confirmed by histopathology in many series.
There is increasing evidence that multidisciplinary management of patients with
suspected PA is superior to standard obstetric care.16-18,116-119 For such care to be
organized, the diagnosis must be made prenatally. We found that most authors of series
published in the last decade have used both the gray-scale and CDI ultrasound signs to
evaluate retrospectively or prospectively the sensitivity of ultrasound in the prenatal
diagnosis of PA. A recent systematic review and meta-analysis by D'Antonio et al120 of
23 of these studies involving 3707 pregnancies at risk of PA found that the overall
performance of ultrasound is excellent (sensitivity 90.7%; specificity 96.9%), and that
CDI has the best predictive accuracy. However, these studies may overestimate
accuracy because they were conducted in centers specialized in prenatal diagnostics,
and the number of cases of PA diagnosed prenatally were small. Out of the 22 series
from D'Antonio et al review that were also included in the present review, eight did not
present with information on the depth of villous invasion 58,59,62,67,71,72,81,82 and one did
not present any histopathologic data at all.85 This suggests that many imaging specialty
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centers may not have access to specialist perinatal pathology. Overall, only three of the
series included in our review provided with a full correlation between standard 2D
ultrasound signs and PA grading, and were included in Table 4.65,84,102 More prospective
studies with detailed evaluation of the depth of accreta placentation at delivery are
needed to better evaluate the accuracy of these ultrasound signs not only in screening
for PA, but also in differentiating between the different levels of depth of myometrial
invasion.
Around 75% of women with PA included in the present review were managed
with planned CD hysterectomy. However, in more than half of these cases, the depth of
villous invasiveness was not described. In those series in which all99, or a high
proportion75,80,87,95 of cases were successfully treated conservatively without the need
for a secondary hysterectomy, it cannot be established if the corresponding PA cases
were mainly superficially adherent to the myometrium or truly invasive. Ideally, the
standard of reference for the different grading of PA is confirmation of the final histology
after hysterectomy has been performed. The quality of the pathological examination is
essential to provide feedback on the accuracy of the prenatal diagnosis of PA. A
standardized method for gross and microscopic pathological examination of
hysterectomy specimens with PA has recently been proposed121, and likewise the
standardized ultrasound descriptions of abnormally invasive placenta22,24 should be
used in the study design of further studies. Hysterectomy is not always clinically
required as the bleeding can be avoided or controlled using conservative methods. In
cases where a final histopathology examination is not available, the diagnosis can be
based on detailed clinical information provided at the time of delivery. In women with
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severe PP, where there is deep invasion of the adjacent organs or structures, the
clinical diagnosis is usually straightforward. By contrast, the differential diagnosis
between PC and focal PI can be more difficult, in particular in the absence of
pathological examination. The differential diagnosis between a difficult placental manual
removal and an abnormally adherent placenta is also difficult in the absence of
histopathological confirmation. In their classical study, Irving and Hertig highlighted this
issue, and stated that “placenta accreta is not to be confused with simple retention of
the after-birth either through failure of the normal mechanism of separation in a healthy
uterus or through its imprisonment behind an hour glass contraction”.9 The used of a
standardized clinical terminology and in particular the use of “creta” to define abnormally
adherent PA and increta and percreta to describe abnormally invasive forms PA is
essential to the precise evaluation of perinatal data.
Histopathologically, PA is now universally defined by a partial or complete
absence of decidua basalis, resulting in placental villi being attached to or invading the
scarred myometrium underneath.1,3,4 Luke et al21 argued against the classification of PA
proposed by some pathologists, and the further subdivision of PA into total and partial
or focal, on the basis that the histological examination in cases of abnormally adherent
placenta is “often distorted by attempt at manual placental delivery and/or post-partum
uterine curettage”. In these cases, the utero-placental interface is inevitably damaged,
impairing the histological examination and making it impossible to make the diagnosis of
abnormal adherent placenta or PC and evaluate its lateral extension. Deeper invasion
of the trophoblast into the myometrium and infiltration of chorionic villi into myometrial
vascular spaces have recently been documented in PI and PP.122 These changes
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provoke a shift in placental blood supply from a spiral artery as found in normal
placentation to a supply from larger, deeper arteries, i.e. radial or arcuate, in abnormally
invasive placentas. These major transformations of the uteroplacental circulation can
explain the high frequency of profound vascular alterations, such as placental blood
lacunae caused by blood entering the placenta at high velocity89 and
hypervascularisation patterns under the placental bed found on ultrasound in PI and PP
(Table 4). These findings suggest that the more invasive the placentation the more
pronounced the utero-placental vascular changes are, and confirms the value of CDI in
the screening of PA and in the evaluation of the depth of villous myometrial invasion.
MRI is increasingly used for the diagnosis of PA and has been reported to be
useful in assessing the depth and lateral extension of myometrial invasion, especially
with posterior placentation andor in obese women. Recent systematic reviews have
found that prenatal MRI is highly accurate in diagnosing disorders of invasive
placentation and that ultrasound and MRI have comparable predictive accuracy.123,124
However, cost and limited access to MRI makes it impractical as a screening tool for PA
and ultrasound imaging remains the primary screening tool for population-based
studies.
Conclusions and implications
With the increasing numbers of CD worldwide and the long-term consequences of
uterine scars, accurate prenatal diagnosis is a pivotal factor in optimizing the
counseling, treatment, and outcome of women presenting with PA. Determining the
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depth and extension of accreta placentation is essential in planning individual
management. Ultrasound sings of PA have a rather subjective quality and may not be
reproducible. The use of different ultrasound equipment used may also influence the
results of ultrasound examinations. Many series published in the literature over the last
three decades do not provide detailed data linking prenatal ultrasound signs and clinical
and histopathological findings at delivery. In addition, the inclusion of the three grades
of accreta placentation into one category has led to heterogeneous data which are
difficult to interpret. This can explain the major variability in terms of prenatal diagnosis
accuracy, outcome and management in specialist centres, and can also explain why
antenatal detection rates remain low in recent general population studies.
Pathological studies and the data of the present review suggest that PA should
be separated into abnormally adherent and abnormally invasive placental tissues as
these are anatomically different entities with different clinical outcomes. The term
“morbidly adherent placenta” is inaccurate and misleading and should refer only to the
first degree of accreta placentation where the villi simply adhere to the myometrium. PI
and PP represent the most severe degree of PA and should be referred to as
abnormally invasive placentation. We therefore recommend that sonographers use the
term placenta “creta” if they think placentation is superficial and invasive if they think it is
deep to discriminate when they are reporting their ultrasound findings. Further
prospective studies that present for each individual case standardised ultrasound signs
and complete clinical and pathological data are now essential to take the prenatal
screening of PA from specialist centres to the general population, and to improve the
outcome of this increasingly common major obstetric complication.
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Table 1: Ultrasound signs identified in the diagnosis of 38 cases reports ranked
according to the depth of villous myometrial invasion.
Ultrasound signs PC PI PP
n(%) n(%) n(%)
Grey-scale Parameters (n=13) (n=16) (n=9)
Loss of clear zone 12(92.3) 14(87.5) 5(55.6)
Myometrial thinning 6(46.2) 11(68.8) 3(33.3)
Placental lacunae 5(38.5) 9(56.3) 9(100)
Bladder wall interruption 1(7.7) 2(12.5) 2(22.2)
Placental bulge - 1(12.5) 1(11.1)
Focal exophytic mass - - 1(11.1)
CDI Parameters (n=11) (n=11) (n=8)
Uterovesical hypervascularity 1(9.1) 2(18.2) 2(25.0)
Subplacental hypervascularity 5(45.5) 9(81.8) 6(75.0)
Bridging vessels 10(90.9) 7(63.6) 2(25.0)
Lacunae feeder vessels 2(18.2) 6(55.5) 4(50.0)
CDI= Color Doppler Imaging; PC= placenta creta or vera; PI= placenta increta; PP= placenta percreta.
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Table 2: Distribution of the ultrasound sign used in the diagnosis of PA in 53 series.
Ultrasound signs n (%)
Grey-scale Parameters (n=52)
Loss of clear zone 50(98.0)
Myometrial thinning 34(66.7)
Placental lacunae 49(96.1)
Bladder wall interruption 30(58.8)
Placental bulge 11(22.0)
Focal exophytic mass 13(25.5)
CDI Parameters (n=42)
Uterovesical hypervascularity 20(47.6)
Subplacental hypervascularity 36(85.7)
Bridging vessels 26(61.9)
Lacunae feeder vessels 22(52.4)
CDI= Color Doppler Imaging
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Table 3: Distribution of standard ultrasound signs found in eight studies presenting detailed data on depth of villous myometrial invasion. Variables References
65 79 84 89 95 98 102 107 T
n n n n n n n n n
No of cases 15 10 9 41 26 32 10 9 152
Placental grading n
PC 8 8 5 15 16 16 3 1 72
PI 3 1 3 9 -- 12 4 2 34
PP 4 1 1 17 10 4 3 6 46
Grey-scale Parameters %
Loss of clear zone 7 10 4 37 23 20 5 69.7
Myometrial thinning 19 32 3 51.0
Placental lacunae 10 10 5 30 23 28 5 9 78.9
Bladder wall interruption 3 15 16 1 23.0
Placental bulge 1 9 6.6
Focal exophytic mass 1 11 7.9
CDI Parameters (n= 128) %
Uterovesical hypervascularity 11 30 2 6 11.3
Subplacental hypervascularity 10 30 7 36.7
Bridging vessels 12 9.3
Lacunae feeder vessels 5 6 8.6
CDI= Color Doppler Imaging; ; PC= placenta creta or vera; PI= placenta increta; PP= placenta percreta. References 65 and 83 included only grey-scale imaging data.
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Table 4: Ultrasound signs identified in the diagnosis of 38 cases reports and in 3 series65,84,102 including 34 cases ranked according to the depth of villous myometrial invasion.
Ultrasound signs PC PI PP
n(%) n(%) n(%)
Grey-scale Parameters (n=29) (n=26) (n=17)
Loss of clear zone 18(62.1) 22(84.6) 8(47.1)
Myometrial thinning 6(20.7) 12(46.2) 4(23.5)
Placental lacunae 16(55.2) 16(61.5) 14(82.4)
Bladder wall interruption 2(6.9) 2(7.7) 5(29.4)
Placental bulge - 1(3.9) 2(11.8)
Focal exophytic mass - - 2(11.8)
CDI Parameters (n=14) (n=15) (n=11)
Uterovesical hypervascularity 3(21.4) 2(13.3) 2(18.2)
Subplacental hypervascularity 5(35.7) 9(60.0) 6(54.5)
Bridging vessels 10(71.4) 7(46.7) 2(18.2)
Lacunae feeder vessels 4(28.6) 8(53.3) 5(45.5)
CDI= Color Doppler Imaging; PC= placenta creta or vera; PI= placenta increta; PP= placenta percreta.
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Figure legend Fig 1: Flow diagram for the selection of cases reports and series on ultrasound imaging of PA.